After several seasons of hard work, the team were promoted into the East Riding Amateur League, they won the championship five consecutive times during the 1950s.

In 1960–61 they reached the First Round proper of the FA Cup eventually losing out to Bishop Auckland who were very strong at the time.

Unfortunately for Bridlington, they were unable to put the icing on the cake in their FA Vase final clash at Wembley with Yeading, they drew the game, but lost in the replay 1–0 at Elland Road.

The 1992–93 season was the most successful in the club's history, they finished as champions of the NPL Division One, and they finally took the FA Vase at Wembley, beating Tiverton Town 1–0.

Due to legalities, the team was forced to play their home games at Doncaster Rovers' ground; Belle Vue.

A local pub team The Greyhound, approached the lease-holders of Bridlington Town's former stadium Queensgate, looking for it to become their base.

And they also reached the Fourth Qualifying Round of the FA Cup, eventually losing to Conference National side Southport.

In 2007, it was announced that Bridlington Town would play in the inaugural season of the Northern Premier League Division One North.

In 2012, The Seasiders won the East Riding Senior Cup, beating Hall Road Rangers (res) 9–2 in the final at the KC Stadium.

Marshall was replaced by the management team of Ash Berry and Paul Stoneman, with the help of Coach Grant Crookes.

Season Chairman Peter Smurthwaite appoints Tim Hotte and Gary Allanson as joint managers, and the club finishes in fourth position in the league.

They lost to UniBond Premier side North Ferriby in the East Riding senior cup final at the KC Stadium, and within days, the management team had resigned from the club for personal reasons.

Due to players leaving, the club finished 12th in the NCEL and lost 5–2 to North Ferriby in the senior cup final.

Another season under Allanson had the team finish in eighth place in the league, but some silverware[clarification needed] in the East Riding Senior cup after a 4–2 win against Hull United where Craig Hogg scored a hat-trick.

It was after a 3–1 away win at Harrogate Railway that the club was shocked by the news that Allanson announced he would be leaving for personal reasons, Chairman Peter Smurthwaite acted swiftly and appointed former professional footballer and British boxing champion Curtis Woodhouse, along with former Hull City Legend Ian Ashbee as his assistant.

Inspirational assistant manager Ian Ashbee left the club and was replaced by former Seasiders player Mally Parker.

Players including Nicky McNamara, Jamie Forrester, and Brett Agnew, were injured on the opening day of the season.

Local player Jake Day scored 48 goals and finished as the top scorer in the NCEL Premier division.

Town finished ninth in the league, who lost in the league cup semi-final to AFC Mansfield and reaching the East Riding Senior Cup final, losing 2–1 to Hull City at the East Riding FA headquarters.Since the departure of Curtis Woodhouse, the team had been managed by aspiring caretaker manager Brett Agnew, along with assistant Anthony Bowsley.

The Seasiders finished third place in the league and won the East Riding Senior Cup Final against Hull City u23s 3–1.

The club won against Dunston FC, meaning the Seasiders would be in the Northern Premier league East division for another season.